Abstract
Urbanization is a process that heavily alters marine and terrestrial environments, though terrestrial urban ecosystems have been studied far more intensively. Terrestrial studies suggest that urbanization can facilitate mesopredators by enhancing food and shelter resources and reducing predation pressure from apex consumers. This in turn has considerable consequences for ecological communities. We evaluated spatial distribution patterns and habitat-use of the marine mesopredator, giant Pacific octopus (Enteroctopus dofleini), relative to terrestrial urbanization intensity in Puget Sound, Washington, USA. Using field surveys and citizen-contributed data for E. dofleini, we examined whether: (1) Distribution was related to urbanization, (2) Abundance was related to the extent of benthic anthropogenic debris, and (3) Diet differed as a function of urbanization and den cover. Our results suggest that urbanization impacts may differ with depth. Mixed-effects logistic regression model estimates for the probability of occurrence increased with urbanization in deep-water (> 24 m), and decreased with urbanization in shallow water (< 18 m). Accompanying field surveys indicated that E. dofleini abundance was correlated with the number of benthic anthropogenic debris items, and that E. dofleini diets were not affected by urbanization intensity or den cover. Though E. dofleini may be synanthropic within certain urban environments, the mechanisms driving this pattern likely differ from those affecting common urban mesopredators on land, with den provisioning from man-made structures being more important than altered food resources.
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References
Alberti M (2008) Advances in urban ecology: integrating humans and ecological processes in urban ecosystems. Springer, Boston
Alberti M, Booth D, Hill K et al (2007) The impact of urban patterns on aquatic ecosystems: An empirical analysis in Puget lowland sub-basins. Landsc Urban Plan 80:345–361. https://doi.org/10.1016/j.landurbplan.2006.08.001
Alberti M, Marzluff J, Hunt VM (2017) Urban driven phenotypic changes: empirical observations and theoretical implications for eco-evolutionary feedback. Philos Trans R Soc B Biol Sci 372:20160029. https://doi.org/10.1098/rstb.2016.0029
Ambrose RF (1983) Midden formation by octopuses: The role of biotic and abiotic factors. Mar Behav Physiol 10:137–144. https://doi.org/10.1080/10236248309378613
Anderson RC (2003) A preliminary report on bioaccumulation in octopuses (Enteroctopus dofleini). In: Proceedings of the 2003 Georgia Basin/Puget Sound Research Conference, March 31-April 3, 2003. British Columbia, Vancouver, pp 1–5
Anderson RC, Mather JA (2010) It’s all in the cues: octopuses (Enteroctopus dofleini) learn to open jars. Ferrantia 59:8–13
André M, Solé M, Lenoir M et al (2011) Low-frequency sounds induce acoustic trauma in cephalopods. Front Ecol Environ 9:489–493. https://doi.org/10.1890/100124
Arce AM, Aguilar-Dávila W, Sosa-Cordero E, Caddy JF (1997) Artificial shelters (casitas) as habitats for juvenile spiny lobsters Panulirus argus in the Mexican Caribbean. Mar Ecol Prog Ser 158:217–224. https://doi.org/10.3354/meps158217
Aronson RB (1986) Life-History and Den Ecology of Octopus-Briareus Robson in a Marine Lake. J Exp Mar Biol Ecol 95:37–56. https://doi.org/10.1002/2015GB005260/full
Aronson MFJ, La Sorte FA, Nilon CH et al (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc Biol Sci 281:20133330. https://doi.org/10.1098/rspb.2013.3330
Bateman PW, Fleming PA (2012) Big city life: Carnivores in urban environments. J Zool 287:1–23. https://doi.org/10.1111/j.1469-7998.2011.00887.x
Beger M, Grantham HS, Pressey RL et al (2010) Conservation planning for connectivity across marine, freshwater, and terrestrial realms. Biol Conserv 143:565–575. https://doi.org/10.1016/j.biocon.2009.11.006
Bishop MJ, Mayer-Pinto M, Airoldi L, Firth LB, Morris RL, Loke LH, Hawkins SJ, Naylor LA, Coleman RA, Chee SY, Dafforn KA (2017) Effects of ocean sprawl on ecological connectivity: impacts and solutions. J Exp Mar Biol Ecol 492:7–30.
Bolnick DI, Yang LH, Fordyce JA et al (2002) Measuring Individual-Level Resource Specialization. Ecology 83:2936–2941
Bolton D, Mayer-Pinto M, Clark GF et al (2017) Coastal urban lighting has ecological consequences for multiple trophic levels under the sea. Sci Total Environ 576:1–9. https://doi.org/10.1016/j.scitotenv.2016.10.037
Briones-Fourzàn P, Lozano-Álvarez E (2001) Effects of artificial shelters (Casitas) on the abundance and biomass of juvenile spiny lobsters Panulirus argus in a habitat-limited tropical reef lagoon. Mar Ecol Prog Ser 221:221–232. https://doi.org/10.3354/meps221221
Bulleri F (2006) Is it time for urban ecology to include the marine realm? Trends Ecol Evol 21:658–659
Bulleri F, Chapman M (2010) The introduction of coastal infrastructure as a driver of change in marine environments. J Appl Ecol 47:26–35
Cohen J (1960) A Coefficient of Agreement for Nominal Scales. Educ Psychol Meas 20:37–46. https://doi.org/10.1177/001316446002000104
Cooper W (2014) Relative index of abundance from visual order-of-magnitude REEF surveys applied to Hogfish (Lachnolaimus maximus) in the Southeast US. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, St. Petersburg, p 29
Crooks K, Soulé M (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566. https://doi.org/10.1038/23028
Dafforn KA, Glasby TM, Airoldi L et al (2015) Marine urbanization: An ecological framework for designing multifunctional artificial structures. Front Ecol Environ 13:82–90. https://doi.org/10.1890/140050
Dafforn KA, Kelaher BP, Simpson SL et al (2013) Polychaete Richness and Abundance Enhanced in Anthropogenically Modified Estuaries Despite High Concentrations of Toxic Contaminants. PLoS One. https://doi.org/10.1371/journal.pone.0077018
Deng JS, Wang K, Hong Y, Qi JG (2009) Spatio-temporal dynamics and evolution of land use change and landscape pattern in response to rapid urbanization. Landsc Urban Plan 92:187–198. https://doi.org/10.1016/j.landurbplan.2009.05.001
Dethier MN, Raymond WW, McBride AN et al (2016) Multiscale impacts of armoring on Salish Sea shorelines: Evidence for cumulative and threshold effects. Estuar Coast Shelf Sci 175:106–117. https://doi.org/10.1016/j.ecss.2016.03.033
Dodge R, Scheel D (1999) Remains of the prey-Recognizing the midden piles of Octopus dofleini (Wulker). The Veliger 42:260–266
Duduś L, Zalewski A, Kozioł O et al (2014) Habitat selection by two predators in an urban area: The stone marten and red fox in Wrocław (SW Poland). Mamm Biol 79:71–76. https://doi.org/10.1016/j.mambio.2013.08.001
Feist BE, Levin PS (2016) Novel Indicators of Anthropogenic Influence on Marine and Coastal Ecosystems. Front Mar Sci 3:1–13. https://doi.org/10.3389/fmars.2016.00113
Fortin M-J, Dale MRT (2005) Spatial analysis : a guide for ecologists. Cambridge University Press, Cambridge
Galgani F, Hanke G, Maes T (2015) Global Distribution, Composition, and Abundance of Marine Litter. In: Bergmann M, Gutow L, Klages M (eds) Marine anthropogenic litter. Springer, New York, pp 29–56
Galgani F, Leaute JP, Moguedet P et al (2000) Litter on the sea floor along European coasts. Mar Pollut Bull 40:516–527. https://doi.org/10.1016/S0025-326X(99)00234-9
Gaston KJ, Davies TW, Bennie J, Hopkins J (2012) Reducing the ecological consequences of night-time light pollution: Options and developments. J Appl Ecol 49:1256–1266. https://doi.org/10.1111/j.1365-2664.2012.02212.x
Gehrt SD, Riley SPD, Cypher BL (2010) Urban carnivores: ecology, conflict, and conservation. Johns Hopkins University Press, Baltimore
George SL, Crooks KR (2006) Recreation and large mammal activity in an urban nature reserve. Biol Conserv 133:107–117. https://doi.org/10.1016/j.biocon.2006.05.024
Hartwick EB, Ambrose RF, Robinson SMC (1984) Dynamics of shallow-water populations of Octopus dofleini. Mar Biol 82:65–72
Heery EC, Bishop MJ, Critchley LP et al (2017) Identifying the consequences of ocean sprawl for sedimentary habitats. J Exp Mar Biol Ecol 492:31–48. https://doi.org/10.1016/j.jembe.2017.01.020
Inglis GJ, Kross JE (2000) Evidence for systemic changes in the benthic fauna of tropical estuaries as a result of urbanization. Mar Pollut Bull 41:367–376. https://doi.org/10.1016/S0025-326X(00)00093-X
Ioakeimidis C, Zeri C, Kaberi H et al (2014) A comparative study of marine litter on the seafloor of coastal areas in the Eastern Mediterranean and Black Seas. Mar Pollut Bull 89:296–304. https://doi.org/10.1016/j.marpolbul.2014.09.044
Katsanevakis S, Verriopoulos G (2004a) Den ecology of Octopus vulgaris Cuvier, 1797, on soft sediment: availability and types of shelter. Ecology 68:147–157. https://doi.org/10.4028/www.scientific.net/KEM.314.213
Katsanevakis S, Verriopoulos G (2004b) Abundance of Octopus vulgaris on soft sediment. Distribution 68:553–560. https://doi.org/10.3989/scimar.2004.68n4553
Kelly RP, O’Donnell JL, Lowell NC et al (2016) Genetic signatures of ecological diversity along an urbanization gradient. PeerJ 4:e2444. https://doi.org/10.7717/peerj.2444
Krishnakumar PK, Casillas E, Varanasi U (1994) Effect of environmental contaminants on the health of Mytilus edulis from Puget Sound, Washington, USA. I. Cytochemical measures of lysosomal responses in the digestive cells using automatic image analysis. Mar Ecol Prog Ser 106:249–261. https://doi.org/10.3354/meps106249
Kwon I, Kim T (2015) Growth and mortality of the juvenile common octopus (Octopus vulgaris) in pipe-and tire-type shelters placed in flow-through seawater tanks. J Kor Soc Fish Technol 51:1–8. https://doi.org/10.3796/KSFT.2015.51.1.001
Legendre P, Anderson MJ (1999) Distance-Based Redundancy Analysis: Testing Multispecies Responses in Multifactorial Ecological Experiments. Ecol Monogr 69:1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Leite AS, Santos LL, Costa Y, Hatje V (2014) Influence of proximity to an urban center in the pattern of contamination by marine debris. Mar Pollut Bull 81:242–247. https://doi.org/10.1016/j.marpolbul.2014.01.032
Long ER, Chapman PM (1985) A Sediment Quality Triad: Measures of sediment contamination, toxicity and infaunal community composition in Puget Sound. Mar Pollut Bull 16:405–415. https://doi.org/10.1016/0025-326X(85)90290-5
Long ER, Dutch M, Weakland S et al (2013) Quantification of pharmaceuticals, personal care products, and perfluoroalkyl substances in the marine sediments of Puget Sound, Washington, USA. Environ Toxicol Chem 32:1701–1710. https://doi.org/10.1002/etc.2281
Luck M, Wu J (2002) A gradient analysis of urban landscape pattern: A case study from the Phoenix metropolitan region, Arizona, USA. Landsc Ecol 17:327–339. https://doi.org/10.1023/A:1020512723753
Magle SB, Lehrer EW, Fidino M (2016) Urban mesopredator distribution: Examining the relative effects of landscape and socioeconomic factors. Anim Conserv 19:163–175. https://doi.org/10.1111/acv.12231
Magle SB, Simoni LS, Lehrer EW, Brown JS (2014) Urban predator-prey association: coyote and deer distributions in the Chicago metropolitan area. Urban Ecosyst:875–891. https://doi.org/10.1007/s11252-014-0389-5
Mann T, Martin AW, French M (1988) Entry of pollutants from seawater into the spermatophore and spermatozoa of the giant octopus of the North Pacific. Mar Pollut Bull 19:669–671. https://doi.org/10.1016/0025-326X(88)90387-6
Mather JA (1994) “Home”choice and modification by juvenile Octopus vulgaris (Mollusca: Cephalopoda): specialized intelligence and tool use? J Zool 233:359–368
McClain CR, Balk MA, Benfield MC et al (2015) Sizing ocean giants: patterns of intraspecific size variation in marine megafauna. PeerJ 3:e715. https://doi.org/10.7717/peerj.715
McDonald PS, Essington TE, Davis JP et al (2015) Distribution, Abundance, and Habitat Associations of a Large Bivalve (Panopea Generosa) in a Eutrophic Fjord Estuary. J Shellfish Res 34:137–145. https://doi.org/10.2983/035.034.0117
McKinney ML (2002) Urbanization, Biodiversity, and Conservation. Bioscience 52:883–890
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Miller MA, Byrne BA, Jang SS et al (2010) Enteric bacterial pathogen detection in southern sea otters (Enhydra lutris nereis) is associated with coastal urbanization and freshwater runoff. Vet Res. https://doi.org/10.1051/vetres/2009049
Narvarte M, González RA, Storero L, Fernandez M (2013) Effects of competition and egg predation on shelter use by Octopus tehuelchus females. Mar Ecol Prog Ser 482:141–151
Neumann B, Vafeidis AT, Zimmermann J, Nicholls RJ (2015) Future coastal population growth and exposure to sea-level rise and coastal flooding - A global assessment. PLoS One. https://doi.org/10.1371/journal.pone.0118571
Prange S, Gehrt SD (2004) Changes in mesopredator-community structure in response to urbanization. Can J Zool 82:1804–1817. https://doi.org/10.1139/z04-179
Prange S, Gehrt SD, Wiggers EP (2003) Demographic Factors Contributing to High Raccoon Densities in Urban Landscapes. J Wildl Manag 67:324–333
Prugh LR, Stoner CJ, Epps CW et al (2009) The rise of the mesopredator. Bioscience 59:779–791. https://doi.org/10.1525/bio.2009.59.9.9
PSNERP (2010) Puget Sound Basin PSNERP Database. Puget Sound Nearshore Partnership, Olympia
Rhodes JR, Wiegand T, McAlpine CA et al (2006) Modeling species’ distributions to improve conservation in semiurban landscapes: Koala case study. Conserv Biol 20:449–459. https://doi.org/10.1111/j.1523-1739.2006.00330.x
Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741. https://doi.org/10.1111/j.1365-294X.2006.02907.x
Riley SPD, Riley SPD, Bromley C et al (2007) Anticoagulant Exposure and Notoedric Mange in Bobcats and Mountain Lions in Urban Southern California. J Wildl Manag 71:1874–1884. https://doi.org/10.2193/2005-615
Rochman CM, Browne MA, Underwood AJ et al (2016) The ecological impacts of marine debris: unraveling the demonstrated evidence from what is perceived. Ecology 97:302–312. https://doi.org/10.1890/07-1861.1
Savage C, Leavitt PR, Elmgren R (2010) Effects of land use, urbanization, and climate variability on coastal eutrophication in the Baltic Sea. Limnol Oceanogr 55:1033–1046. https://doi.org/10.4319/lo.2010.55.3.1033
Scheel D (2015) Sea-surface temperature used to predict the relative density of giant Pacific octopuses (Enteroctopus dofleini) in intertidal habitats of Prince William Sound, Alaska. Mar Freshw Res 66:866–876. https://doi.org/10.1071/MF14197
Scheel D, Anderson R (2012) Variability in the diet specialization of Enteroctopus dofleini (Cephalopoda: Octopodidae) in the eastern Pacific examined from midden contents. Am Malacol Bull 30:267–279. https://doi.org/10.4003/006.030.0206
Scheel D, Bisson L (2012) Movement patterns of giant Pacific octopuses, Enteroctopus dofleini (Wülker, 1910). J Exp Mar Biol Ecol 416–417:21–31. https://doi.org/10.1016/j.jembe.2012.02.004
Scheel D, Lauster A, Vincent TLS (2007) Habitat Ecology of Enteroctopus dofleini from Middens and Live Prey Surveys in Prince William Sound, Alaska. In: Landman NH, Davis RA, Mapes RH (eds) Cephalopods Present and Past: New Insights and Fresh Perspectives. Springer, Dordrecht, pp 434–458
Schultz JA, Cloutier RN, Côté IM (2016) Evidence for a trophic cascade on rocky reefs following sea star mass mortality in British Columbia. PeerJ 4:e1980. https://doi.org/10.7717/peerj.1980
Semmens JM, Pecl GT, Gillanders BM et al (2007) Approaches to resolving cephalopod movement and migration patterns. Rev Fish Biol Fish 17:401–423. https://doi.org/10.1007/s11160-007-9048-8
Shochat E, Warren PS, Faeth SH et al (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191. https://doi.org/10.1016/j.tree.2005.11.019
Spirandelli DJ (2014) Examining the effects of wastewater infrastructure on Puget Sound near-shore water quality across a gradient of urbanization. Dissertation, University of Washington
Storero LP, Narvarte MA, González RA (2013) Seasonal density and distribution of Octopus tehuelchus in the intertidal of north Patagonia. J Mar Biol Assoc United Kingdom 93:1895–1901. https://doi.org/10.1017/S0025315413000416
Thiel M, Hinojosa IA, Miranda L et al (2013) Anthropogenic marine debris in the coastal environment: A multi-year comparison between coastal waters and local shores. Mar Pollut Bull 71:307–316. https://doi.org/10.1016/j.marpolbul.2013.01.005
Toft JD, Cordell JR, Simenstad CA, Stamatiou LA (2007) Fish Distribution, Abundance, and Behavior along City Shoreline Types in Puget Sound. North Am J Fish Manag 27:465–480. https://doi.org/10.1577/m05-158.1
Vargas-Fonseca E, Olds AD, Gilby BL et al (2016) Combined effects of urbanization and connectivity on iconic coastal fishes. Divers Distrib 22:1328–1341. https://doi.org/10.1111/ddi.12495
Williams R, Wright AJ, Ashe E et al (2015) Impacts of anthropogenic noise on marine life: Publication patterns, new discoveries, and future directions in research and management. Ocean Coast Manag 115:17–24. https://doi.org/10.1016/j.ocecoaman.2015.05.021
Wolfe JR, Pattengill-Semmens CV (2013) Estimating fish populations from REEF citizen science volunter diver order of magnitude surveys. CalCOFI Rep 54:127–140. https://doi.org/10.1017/CBO9781107415324.004
Yasuhara M, Hunt G, Breitburg D et al (2012) Human-induced marine ecological degradation: Micropaleontological perspectives. Ecol Evol 2:3242–3268. https://doi.org/10.1002/ece3.425
Zhou P, Huang C, Fang H et al (2011) The abundance, composition and sources of marine debris in coastal seawaters or beaches around the northern South China Sea (China). Mar Pollut Bull 62:1998–2007. https://doi.org/10.1016/j.marpolbul.2011.06.018
Acknowledgements
We are grateful to Christy Pattengill-Semmens, the REEF program, and the many divers who made this study possible. Special thanks to Ed Gullekson and Rhoda Green for their invaluable support as advisors and research divers on the project, and to David Thoreson, for building field equipment, captaining, and elevating spirits in the field. We are grateful also to Gregory Jensen for providing guidance on midden identification, and to Megan Dethier, Tim Essington, William King, Jennifer Ruesink, and Stephani Wei for manuscript and/or modeling feedback. NOAA_OI_SST_V2 data was provided by the NOAA/OAR/ESRL PSD, Boulder, Colorado, USA, from their Web site at http://www.esrl.noaa.gov/psd/. PDO data were provided by the NOAA/NESDIS/NCEI, Asheville, North Carolina, USA, from their website at https://www.ncdc.noaa.gov/teleconnections/pdo/. Heery was funded by the National Science Foundation Integrative Graduate Education and Research Traineeship (IGERT) Program on Ocean Change (NSF 1068839, T. Klinger PI, with K Sebens as co-PI). Financial support for this study was also provided by the Biology Department and the School of Aquatic and Fisheries Science at the University of Washington.
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Heery, E.C., Olsen, A.Y., Feist, B.E. et al. Urbanization-related distribution patterns and habitat-use by the marine mesopredator, giant Pacific octopus (Enteroctopus dofleini). Urban Ecosyst 21, 707–719 (2018). https://doi.org/10.1007/s11252-018-0742-1
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DOI: https://doi.org/10.1007/s11252-018-0742-1